Reinforcement mechanisms for auditory perceptual learning - PROJECT SUMMARY/ABSTRACT It is commonly accepted that, when it comes to learning motor skills, such as dancing or sewing, “practice makes perfect.” Less appreciated, however, is that our senses also benefit from practice. With training, we can improve our ability to see, hear, smell, and taste – a process termed perceptual learning (PL). In the auditory system, PL underlies key elements of human social communication, such as speech phoneme discrimination and musicality. In the brain, PL is associated with changes in stimulus representations in sensory cortical regions. However, passive stimulus exposure on its own is not sufficient to induce sensory cortical plasticity or PL, and extensive training is required. Strikingly, if passively presented stimuli are paired with electrical stimulation of the ventral tegmental area (VTA), visual cortical plasticity and improvements in visual perception can occur, suggesting that VTA dopaminergic (DA) signaling may play a critical role in PL, at least in the visual system. The causal role of VTA in auditory PL is entirely unexplored. In associative learning, VTA DA neurons encode prediction errors: early in training, reinforcement, but not the preceding stimulus, drives strong neuronal firing. With training, VTA DA neuronal firing gradually shifts from the now-expected reinforcement towards the preceding stimulus. However, PL differs from associative learning, in that training for PL typically employs progressively weaker renditions of a previously learned stimulus and ultimately results in improved detection. I hypothesize that to improve detection of weak signals, the brain engages the same prediction error mechanisms that support associative learning. I propose that reinforcement cues preceded by weak sounds are encoded as prediction errors and drive VTA DA neurons to fire, thereby generating the improvements in cortical neural sensitivity that give rise to PL. To test if VTA DA neurons signal prediction errors during PL, this proposal will employ fiber photometry and high channel-count electrophysiology to monitor neurons in the VTA as freely moving Mongolian gerbils train on an auditory PL task. Then, VTA DA neurons will be targeted with optogenetic manipulations during behavior to evaluate if gain or loss of function affects PL at the behavioral and auditory cortical levels. This proposal offers the first direct test of whether VTA’s role extends to auditory perceptual learning. My goal is to establish an independent career focused on how reinforcement-dependent neuromodulation results in sustained adaptive changes in auditory circuits. In the long-term, my research could inform the development of strategies to enhance everyday perceptual skills or to improve sensory dysfunction in the hard-of-hearing population.
